Dr Helmuth Zimmerman is the Division Manager for Weeds Research at the Plant ProtectionResearch Institute, South Africa, and Hildeguard Klein is a research technician with the PPRI.

Abstract

The USA and South Africa are among the world’s leading biological weed control countries. By1998,seventy-three biocontrol agents had been released on thirty-six weeds in USA mainlandand by 1999, eighty-two agents on forty-seven weeds in South Africa. The early Hawaiianprojects served as a training school and source of tested biocontrol agents for other countries.In South Africa, nineteen of the target weeds for biocontrol are woody invaders, compared toonly two woody species in USA. Most of the woody invaders in South Africa are economicallyimportant, eliciting conflicts in interest typical of South Africa. The two countries need eachother’s assistance to control invasive species originating from each other’s country, e.g.Delairea odorata Lemaire and Carpobrotus edulis (L.) L. Bol., which are among the top ten weedsin USA, and Prosopis spp., among the worst invaders in South Africa. The USA and South Africaalready co-ordinate their research on certain invasives they have in common, they sharefacilities and co-operate on contract basis. Off-target feeding by some biocontrol agents in bothcountries forced researchers and decision-makers to be more critical, and resulted in therevision of the protocols regarding release of new agents.

Introduction

The USA and South Africa share a common problem with alien plant invasions. Well over 980alien plants had been naturalised in South Africa by 1986 (Wells et al. 1986). Henderson(1995) determined and illustrated 161 of the most important alien plant invaders in thecountry, and a new edition of this field guide, Plant Invaders of Southern Africa (Henderson, inprep.), with 40 additional plant species, is due to be published soon. This publication willcover the complete list of ‘declared weeds’ and ‘invader plants’ referred to in the Conservationof Agricultural Resources Act, 1983 (Act 43 of 1983), the Regulations of which are currentlybeing amended. Of the 200 species covered in the new edition of the field guide, 60 originatefrom South America, 38 from Central America, 32 each from Europe and Asia, 30 fromAustralia, 27 from North America, 5 from elsewhere in Africa and 1 from New Zealand.

Alien plant invaders have been estimated to cover 10 million hectares in South Africa, which

represents about 8% of the surface area of the country. How much these alien plant invasionscost the country has not been determined, except in terms of water losses due to woodyinvaders (Versfeld, Le Maitre & Chapman 1998). It was estimated that, if these invasionscould be cleared over a period of 20 years, the annual cost would amount to some R600million (approximately US$1 m). The current biological control programmes have alreadyreduced the present amount by 19.8%.

This represents an overall saving of R1.38 billion.The potential savings, if biocontrol were to be exploited fully, are estimated at 58.6% or R4.08billion (Versfeld et al. 1998). Biological control should therefore be considered to be anindispensable component in the control of alien plant invaders in South Africa.In South Africa, the Working for Water Programme of the Department of Water Affairs andForestry has taken the initiative to pursue the goal of ridding the country of alien invasiveplants. Considerable progress has already been made. In the USA, these efforts arematched by an Executive Order recently announced by President Bill Clinton, whichaddresses the growing environmental and economic threat of alien invasives. Thesedevelopments pave the way for fruitful co-operation and partnerships, which will be discussedin more detail below.

The alien plant species

By 1998, South Africa had targeted 35 alien weed species for biological control, as comparedto 36 species in mainland USA and 20 species in Hawaii (Julien & Griffiths, 1998). Apublication of a year later gives the South African figure as 47, but no statistics were availablefor the USA at that time (Table 1). Most of the plants targeted for biological control in SouthAfrica are woody plants, while the majority of projects in the USA target herbaceous weeds(Table 2). This is a major difference between the projects of the two countries. Most of thewoody invaders that are now targeted for biological control in South Africa were onceintroduced deliberately, and therefore their eradication will be fraught with conflicts ofinterests. Although such plants cause problems in certain situations, they are neverthelessbeneficial to a part of the population. Resolving such conflicts has become standardprocedure in most projects involving the biological control of woody invaders in South Africa(Neser & Moran 1986).

Table 3 lists some of the plant species of South African origin that have become invasive in

the USA. Most of these are Mediterranean species of Cape origin that have escaped fromcultivation in California, and two of them (Delairea odorata Lemaire and Carpobrotus edulis(L.) L. Bol.) rank among the country’s top ten weeds (Anderson et at. 1996). Many morespecies are alreadynaturalised but are not yet regarded as weeds in the USA, e.g.Dichrostachys cinerea (L.) Wight & Arn, which is a major problem in Cuba (E. PérezMontesbravo, pers. comm.) and is already naturalised in Florida (Wunderlin 1998).Table 4 lists the most important alien plant invaders in South Africa that are of NorthAmerican origin (Henderson 1995). Among these, mesquite (Prosopis spp.) is by far the mostaggressive species complex in the dry northwestern parts of South Africa, while also causingproblems in other African countries such as Sudan, Somalia and Namibia. Several North

American members of the family Cactaceae are naturalised in South Africa and their control iscosting the country dearly.

The two countries have in common several alien plant invaders from mainly European, outhAmerican, Australian and Asian origin (Table 5). Several of these, such as Sesbania punicea(Cav.) Benth., Paraserianthes lophantha (Willd.) Nielsen, Salvinia molesta D.S. Mitchell,Leptospermumlaevigatum (Gaertn.) F. Muell. and Macfadyena unguis-cati (L.) A. Gentry arebeing controlled biologically in South Africa, and the natural enemies could be made availableto the USA, together with the relevant host-specificity results. Likewise, South Africa madeuse of the research by USA on the biological control of Convolvulus arvensis L (Craemer,Neser & Smith-Meyer 1996) and Eichhornia crassipes (Martius) Solms-Laubach (Cilliers1991).

Biological control

Both countries have a long history of biological weed control, but the pioneering work was

done in Hawaii, which had already released 15 species of biocontrol agents by 1910, beforeany releases were made on mainland USA or South Africa (Julien & Griffiths 1998) (Table 6).The first deliberate release of a biocontrol agent in South Africa was made in 1913 with theintroduction of the South American cochineal, Dactylopius ceylonicus (Green), on the cactusOpuntia vulgaris (Miller) (now O. monocantha) (Neser & Annecke, 1973). The first recordedrelease of a biological control agent in the USA was in 1945 when the leaf-feeding beetle,Chrysolina hyperici (Forster), was used to control St John’s wort (Hypericum perforatumLinnaeus) (Julien & Griffiths 1998). There was a sharp increase in the release of biocontrolagents in both countries from the sixties onwards (Table 6). The earlier campaigns in SouthAfrica relied on the assistance and close co-operation of Australian and Hawaiianentomologists who made natural enemies available to other countries (so-called transferprojects). The first release of a biocontrol agent that was entirely developed and funded bySouth Africa took place in 1948 when the weevil, Metamasius spinolae (Gyllenhal), wasintroduced from Mexico for the biological control of Opuntia ficus-indica (L.) Miller in SouthAfrica (Annecke & Moran 1978).

Hawaii stands out as the country that has pioneered biological weed control. It was the most

active biocontrol country until 1970, having released no fewer than 75 biocontrol agents,compared to only 19 and 29 in South Africa and the USA, respectively (Julien & Griffiths1998). This is understandable in view of the severe threats that alien plant invaders pose tothe unique biodiversity of that highly invaded island. The experience gained in Hawaiiregarding the new science of biological weed control was profitably applied in many othercountries. Most of the early biological control agents released on weeds such as L. Camarawere imported from Hawaii.

Conflicts of interest

The issue of conflicts of interest in biological weed control has been an important determinantfor the direction that research in South Africa is currently taking. Approximately 20 of the 50most important invaders were deliberate introductions, comprising agroforestry species,fodder plants, dune stabilisers, fruit and hedge plants and garden ornamentals (Macdonald,Kruger & Ferrar 1986). Their biological control will always elicit strong oppositions fromspecific interest groups. This problem is addressed through consultation with the relevantinterest groups and through their participation in research activities concerning the biologicalcontrol of such target plants (Zimmermann & Neser 1999).

The biological control of certain commercial forestry species such as Acacia mearnsii De

Wild, Acacia melanoxylon R. Br., Prosopis spp. and Pinus spp. is a sensitive issue, and thislimits biological control options to the use of seed destroying insects (Neser & Kluge 1986).During the late 1980s, the imminent release of the seed-feeding weevil, Melanterius sp. Nearmaculatus, intended to eliminate the annual seed crop of the commercial forestry species,Acacia mearnsii, provoked a strong reaction from the forestry industry in South Africa(Stubbings 1977). Evidence had to be provided that seed orchards could be protected fromthe seed-feeders before the industry would support the release of the insects (Donnelly, Calitz& Van Aarde 1992). The use of host-specific seed-feeding biocontrol agents is now widelyaccepted by the forestry industry as a means of curtailing the unwanted spread of exotic,commercial, forestry species.

We have now started to research the feasibility of introducing cone and pine seed feeders toprevent invasion by several commercial pine species, including Pinus radiata D. Don., whichis of Californian origin. These projects against commercial species would not be possiblewithout an understanding within the forestry fraternity of the basic ecological issues ofbiological weed control or without their confidence in the scientific integrity of the research. Inthis respect, South Africa is far advanced in addressing the problem of conflict of interest inbiological weed control.

In contrast, this level of conflict is not yet a major issue in the USA, and the only recent casewas the biological control project against saltcedar (Tamarix spp.). The release of the firstbiological control agent against saltcedar was long delayed for fear that it might affect anendangered subspecies of a willow flycatcher. This bird species learned to nest in thesaltcedar after this tree had displaced its native nesting trees (DeLoach et al. 1996). This isone of the only two woody invasive trees that are being targeted for biological control in theUSA, the other being Melaleuca quinquenervia (Cav.) S.T. Blake. Conflict resolution hasbecome a major issue in biological weed control and both our countries can learn valuablelessons from the experience of one another.

Another source of conflict emerged more recently when certain biocontrol agents started tofeed and develop on native, non-target species, although this had been predicted at the timeof release. A recent case study from the USA is Rhinocyllus conicus (Frölich), introduced forthe biological control of introduced European thistles but now feeding on and threateningnative Cirsium species (Louda et al. 1997). The advantages of controlling this invaderoutweighed the limited non-target effects that were predicted at that time.

Similarly, in South Africa, the decision to release Dactylopius opuntiae (Cockerell) andCactoblastis cactorum (Bergroth) for the control O. ficus-indica was taken despite the warningthat both insects would damage the spineless varieties of cactus pear (Pettey 1948). Theenormous benefits of biologically controlling this plant, which was regarded as a nationaldisaster at that time, outweighed the predicted damage to the spineless varieties. Today, theenormous benefits derived from biological control have long been forgotten, but we arereminded almost daily of the two pests that need to be controlled on commercial spinelesscactus pear plantations (Annecke & Moran 1978). The decision of 1932 to release these twoinsects is now perceived by an increasing number of cactus pear farmers to have been amistake, although at that time it was the farmer lobby in parliament that insisted on therelease of these insects. We would do well to take note that perceptions and values changeover time.

Hundreds of new exotic forestry and agroforestry tree species are being introduced andcultivated in Africa and elsewhere, where they are now perceived as being beneficial to theenvironment. Some of these will, no doubt, soon change into environmental disasters unlesswe act promptly. Biocontrol researchers in South Africa advocate the idea of introducingeffective, host-specific seed-feeders at an early stage of the establishment of newagroforestry and forestry species as part of the development project, as suggested by Hughes(1995). This applies particularly to developing countries, which are unlikely to have theresources for control costs.

The prediction of aggressive behaviour in newly introduced plants is an important newscience that will assist developers in deciding which plant species to introduce and againstwhich plant species early measures should be taken to prevent unwanted invasion. Cooperativeresearch between South Africa and the USA has pioneered this very importantconcept (Rejmanek 1996).

Success rating in biological weed control

The success rate of agent establishment and impact on weed populations in South Africa

(Olckers & Hill 1999) compares favourably with that of the USA and Hawaii. At least eightinvasive species (17% of the weeds targeted for biological control) are regarded as beingunder complete biological control in South Africa, and a further fourteen species (30%) areunder substantial biological control in the sense that conventional control is still needed, but atreduced rates. In four species (8%), biological control is negligible since there has beenvirtually no reduction in conventional control methods, despite damage inflicted by the agent.For the remainingtwenty-one species (45%), the programmes have either never beenevaluated or the release of the agents have been too recent to allow meaningfulassessments.

The failure of agents to qualify for release after several years’ research investment, or their

release and subsequent non-establishment, are drawbacks of this discipline. South Africa canill afford to waste expensive research capacity and financial resources on ‘losers’. Althoughthe long history of biological weed control, with some 370 species released world wide (Julien& Griffiths 1998), has provided scientists with a data base from which to draw conclusions,the selection of potential successful biocontrol agents is still mostly based on ‘instinct’ ratherthan on rational arguments. It would appear as if the prediction of ‘winners’ or ‘losers’ inbiological weed control is beginning to attract more attention among researchers, and this willhopefully succeed in rendering research programmes more cost-effective.

Partnerships

It has become increasingly difficult to gain access to the fauna and flora of some of thecountries of origin of our alien weeds, and even more difficult to export potential biocontrolagents. Property rights and the potential commercial value of the national flora, fuelled byCITES and other agreements, often prevent foreign exploration which is the lifeline ofbiological weed control. A sensible development has been the forging of partnerships withthose countries and the utilisation of local expertise and capacity to carry out some of theexploration and host-specificity research.

Such a partnership is already in existence between South Africa and the USA. South Africais engaged in an extensive survey of all associated insects, mites and fungi on the Cape ivy,Delairea odorata Lemaire, which is a major invader in California. Another opportunity forsimilar co-operation would be to contract South Africans to survey here for natural enemiesof the Old World climbing fern, Lygodium microphyllum Swartz, which is threatening theindigenous vegetation of the USA. It makes sense for the USA to utilise local knowledge,including taxonomic services, plant identification and distribution, dealing with localauthorities, and safety issues, provided that the quality of services is of the highest standard.

South Africa developed expertise on the biological control of Solanum species in the courseof its research on S. elaeagnifolium Cav., S. sisymbriifolium Lam. and S. mauritianum Scop.(Olckers et al. 1999; Olckers 1999). We are, in fact, the only country that has releasedbiocontrol agents on any Solanum species. This expertise is placed at the disposal ofresearchers in Florida, USA, who are faced with the problem of controlling Solanum viarumDunal. South Africa has similar partnerships with Australia and CABI in the United Kingdom.

Inversely, South Africa is desperately in need of collaboration with USA partners in aresearch programme to select and test suitable biocontrol agents against one of our worstplant invaders, viz. mesquite (hybrid populations between Prosopis velutina Wooton and P.glandulosa var. torreyana (L. Benson) M.C. Johnston). For practical reasons, most of theresearch will have to be done in the native range of the plants, namely in Texas, New Mexicoand Arizona. Thus far, the prohibitive costs have prevented us from launching the project.Other weeds of USA origin (Table 4) that need to be researched are Rubus cuneifoliusPursh. (bramble), the Lantana camara L. complex, Solanum elaeagnifolium Cavanilles andvarious cactus species such as Opuntia rosea DC and Opuntia humifusa (Raf.) Raf. (= O.compressa (Salisb.) Macbride).

The sharing of overseas facilities and expertise to survey and study natural enemies forbiological control is important to ensure low costs and high standards. This is particularlyrelevant where we have invasive species in common. South Africa and the USDA(Gainesville, Florida) are presently sharing the costs of a programme to study the hostspecificityof new promising biocontrol agents against water hyacinth (E. crassipes) in itsnative South America. Similar co-operation on other aquatic weeds such as Myriophyllumaquaticum (Vell.) Verdc. and Pistia stratiotes L. would also be feasible. The USDA biologicalcontrol laboratories in Montpellier have been placed at our disposal should we need toundertake research on weeds of European origin.

We are sharing the concern of our USA counterparts about the inadvertent arrival of the wellknowncactus-feeding moth, Cactoblastis cactorum, in Mexico as this could harm the goodimage of biological weed control and cause irreparable damage to the Opuntia flora of thatcountry (Zimmermann, Moran & Hoffmann in press). Most of the research on C. Cactorumwas done in South Africa as part of the biological control programme against invasive Opuntiaspecies and for protecting commercial cactus pear orchards. This information will be highlyrelevant when control programmes have to be developed to prevent the further invasion ofthis insect into Florida and Mexico.

Strong partnerships amongst the leading countries in biological weed control are important toformulate codes of conduct and safety standards, as illustrated by the co-operative effort inassisting the FAO to compile a code of conduct for the import and release of exotic biologicalcontrol agents (FAO 1996). A proposed code of best practices for classical biocontrol ofweeds, as presented by Balciunas (1999), has now been discussed widely and may lead tothe adoption of common principles.

Conclusions

The most frightening form of globalisation is the movement of exotic plants and animals intovirtually every ecosystem on earth (Bright 1998). Although the deliberate and calculatedtransfer of some of their natural enemies is sometimes seen as compounding the problem,the contrary is, in fact, true in the case of plant control.

Biological weed control often remains the only tool available for some of our worst alien plantinvaders. The long list of successes, involving more than 370 biocontrol agents world wide,is evidence of its potential and safety, notwithstanding a few isolated cases of predicted nontargeteffects. New research results in insect-plant relationships, supported by field evidencefrom biological control of weeds projects, increasingly enable us to improve the safetymargins and allow us to select winners more effectively. Co-operative research projectsshouldreduce costs even further and improve the reliability of results. Countries willincreasingly be guided by international protocols and regional agreements on the release ofbiocontrol agents. More frequent symposia, workshops, student exchanges and meetingsthat focus on particular problems in biological weed control should be encouraged in this fastdeveloping, applied science.

More emphasis should be placed on cost/benefit studies as part of any biological controlproject. The potential savings of biological control was recently estimated as 58.6% of thetotal costs of control, which would amount to R4.08 billion had a once-off treatment beenpossible (Versfeld et al. 1999). Both the South African Working for Water Programme andUSA’s President Clinton have acknowledged this potential by allocating generous funding tothe control of alien plant invaders, which includes biologically based management tactics.

Balciunas, J. (1999) A proposed Code of Best Practice for classical biocontrol of weeds.Abstracts of the X International Symposium on Biological Control of Weeds,Bozeman, Montana, USA. 2-14 July 1999. Montana State University. p. 102.